Explaining variation in individual fitness is a key goal in evolutionary biology. Recently, telomeres, repeating DNA sequences capping the ends of chromosomes, have gained attention as a biomarker for body state, individual quality, and ageing. However, existing research has provided mixed evidence for whether telomere length correlates with fitness components, including survival and reproductive output. Moreover, few studies have examined how telomere shortening correlates with fitness in wild populations. Here, we intensively monitored an insular population of house sparrows on Lundy Island, UK, and collected longitudinal telomere and life history data spanning 16 years from 1,225 individuals. We tested whether telomere length and/or shortening predict fitness measures, namely survival, lifespan, as well as annual and lifetime reproductive success. Telomere length positively predicted immediate survival up to one year after measurement, independent of age, but did not predict lifespan, suggesting either a diminishing telomere length – survival correlation with age, or other extrinsic factors of mortality. The positive effect of telomere length on survival translated to reproductive benefits, as birds with longer telomeres produced more genetic recruits over their lifetime, but not annually, suggesting variation in individual quality. The rate of telomere shortening, however, correlated with neither lifespan nor lifetime reproductive success. Our results provided further evidence that telomere length correlates with fitness, and they contributed to our understanding of how telomere dynamics link with individual quality.

In socially monogamous species, sexual selection not only depends on initial mate choice but also mate switching. To date, studies lack assessment of differences between passive (widowhood) and active (divorce) mate switching, longer-term fitness consequences, and how age masks reproductive costs and benefits of divorce. We investigated causes and long-term consequences of divorce and their age-dependence using longitudinal data on Seychelles warblers (Acrocephalus sechellensis), and experimentally test for short-term effects of mate-switching. Young and old males, but not females, divorced most frequently. Divorce propensity declined with pair bond duration and reproductive success in both sexes, but mate switching did not result in short-term costs. Divorcees did not gain short- or long-term fitness benefits compared to non-divorcees. In fact, female early-life divorcees that lost their breeding position had lower survival than females that never divorced. Divorce is likely a strategy to escape poor-quality partnerships, but not all divorcees benefit from divorcing.

An accurate inference of the chronological and biological age of individuals is fundamental to population ecology and our understanding of ageing itself, its evolution and the biological processes that affect or even cause ageing. In humans, epigenetic clocks based on the DNA methylation (DNAm) at selected CpG sites correlate highly with chronological age. Discrepancies between the inferred epigenetic and known chronological age predict morbidity and mortality, and therefore epigenetic clocks are thought to reflect biological age. Recently, a growing number epigenetic clocks in non-model organisms have been developed towards a diverse array of purposes in commercial, conservation and ageing research. Here we review those studies and conduct the first meta-analysis to assess the effects of different aspects of experimental protocol on the accuracy of epigenetic clocks for non-model species. Our analysis reveals higher coefficients of determination (R2) of chronological age for epigenetic clocks based on the HorvathMammalMethylChip4, compared to other DNAm quantification approaches. No dependence of (R2) was detected for the number of CpG sites in a clock; the sample size; the number or kind of tissue(s) used; the class of animals; or whether captive or wild animals were sampled to infer the epigenetic clocks. We further conclude that epigenetic clocks can predict chronological age with relatively high accuracy, suggesting great potential for the field of ecological epigenetics. We therefore encourage further research on the topic of ecological epigenetics in relation to ageing and, perhaps more importantly, discuss the potential of employing DNAm to assess key traits other than age.

1) The environment experienced during development, and its impact on intrinsic condition, can have lasting outcomes for adult phenotypes and could contribute to the individual variation in senescence trajectories. 2) However, the nature of this relationship in wild populations remains uncertain, owing to the difficulties in summarizing environmental complexity and long-term monitoring of individuals from free-roaming long-lived species. 3) In this study, we determine whether juvenile condition (derived from measures of body mass and size) is associated with senescence-related traits of a closely monitored population of Seychelles warblers (Acrocephalus sechellensis). 4) Juveniles with a higher condition index were more likely to survive to adulthood – suggesting these juveniles experienced better developmental conditions. Furthermore, these juveniles as adults were in better condition and had higher rates of annual survival, independently of age. In contrast, there was no association between juvenile condition and declines in adult telomere length (a measure of somatic stress) nor annual reproduction. 5) These results indicate that juvenile condition, while not associated with senescence trajectories, can influence the likelihood of surviving to old age due to silver-spoon effects. This study shows that measures of intrinsic condition in juveniles can provide important insights into long-term fitness of individuals in wild populations.

Telomeres have been advocated to be important markers of biological age in evolutionary and ecological studies. Telomeres usually shorten with age, and shortening is frequently associated with environmental stressors and increased subsequent mortality. Telomere lengthening – an apparent increase in telomere length between repeated samples from the same individual – also occurs. However, the exact circumstances, and consequences, of telomere lengthening are poorly understood. Using longitudinal data from the Seychelles warbler (Acrocephalus sechellensis), we tested whether telomere lengthening – which occurs in adults of this species – is associated with specific stressors (reproductive effort, food availability, malarial infection and cooperative breeding) and predicts subsequent survival. In females, telomere shortening was observed under greater stress (i.e. low food availability, malaria infection), while telomere lengthening was observed in females experiencing lower stress (i.e. high food availability, assisted by helpers, without malaria). The telomere dynamics of males were not associated with the key stressors tested. These results indicate that, at least for females, telomere lengthening occurs in circumstances more conducive to self-maintenance. Importantly, both females and males with lengthened telomeres had improved subsequent survival relative to individuals that displayed unchanged, or shortened, telomeres – indicating that telomere lengthening is associated with individual fitness. These results demonstrate that telomere dynamics are bidirectionally responsive to the level of stress that an individual faces, but may poorly reflect the accumulation of stress over the lifetime. This study challenges how we think of telomeres as a marker of biological age.

Understanding where and how genetic variation is maintained within populations is important from an evolutionary and conservation perspective. Signatures of past selection suggest that pathogen-mediated balancing selection is a key driver of immunogenetic variation, but studies tracking contemporary evolution are needed to help resolve the evolutionary forces and mechanism at play. Previous work in a bottlenecked population of Seychelles warblers (Acrocephalus sechellensis) show that functional variation has been maintained at the viral-sensing Toll-like receptor 3 (TLR3) gene. Here, we characterise evolution at this TLR3 locus over a 25-year period within the original remnant population of the Seychelles warbler, and in four other derived, contained populations. Results show a significant and consistent temporal decline in the frequency of the TLR3C allele in the original population, and that similar declines in the TLR3C allele frequency occurred in all the derived populations. Individuals (of both sexes) with the TLR3CC genotype had lower survival, and males - but not females - that carry the TLR3C allele had significantly lower lifetime reproductive success than those with only the TLR3A allele. These results indicate that positive selection, caused by an as yet unknown agent, is driving TLR3 evolution in the Seychelles warblers. No evidence of heterozygote advantage was detected. However, whether the positive selection observed is part of a longer-term pattern of balancing selection (through fluctuating selection or rare-allele advantage) cannot be resolved without tracking the TLR3C allele in the populations over an extended period of time.